The spatial structure of genetic diversity underlying social variation is a critical determinant of how cooperation and conflict evolve. Here we investigated whether natural social groups of the cooperative soil bacterium Myxococcus xanthus harbor internal genetic and phenotypic variation and thus the potential for social conflict between interacting cells. Ten M. xanthus fruiting bodies isolated from soil were surveyed for variation in multiple social phenotypes and genetic loci, and patterns of diversity within and across fruiting body groups were examined. Eight of the 10 fruiting bodies were found to be internally diverse, with four exhibiting significant variation in social swarming phenotypes and five harboring large variation in the number of spores produced by member clones in pure culture. However, genetic variation within fruiting bodies was much lower than across fruiting bodies, suggesting that migration across even spatially proximate groups is limited relative to mutational generation of persisting endemic diversity. Our results simultaneously highlight the potential for social conflict within Myxococcus social groups and the possibility of social coevolution among diverse related lineages that are clustered in space and cotransmitted across generations.